Cellular Mechanisms Underlying Activity Patterns in the Monkey Thalamus During Visual Behavior

Ramcharan, Eion J.; Cox, Charles L.; Zhan, Xia; Sherman, S. Murray; Gnadt, James W.

doi:10.1152/jn.2000.84.4.1982

Cited by 43 publications

(25 citation statements)

References 24 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…11 and 38; for review see ref., 39) and in vivo (1,40). These results corroborate other studies that have shown bursting activity during wakefulness in cats (13,14), guinea pigs (15), rabbits (16), and monkeys (17,18). Thus, it is clear that bursting can occur during wakefulness and, indeed, can be observed during periods of sensory processing (12)(13)(14).…”

Section: The Burst Firing Mode Is Not Limited To Sleep and Pathologicsupporting

confidence: 87%

“…11 for review), such as during slow-wave sleep, barbiturate anesthesia, and pathological conditions such as seizure activity. However, it has recently been demonstrated that thalamic bursting can occur during awake states as well, in multiple species (12)(13)(14)(15)(16)(17)(18), and that sensory information can be conveyed to the cortex during the burst activity (16).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Thalamic bursting in rats during different awake behavioral states

Fanselow

Sameshima²,

Baccalá³

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

218

174

View full text Add to dashboard Cite

Thalamic neurons have two firing modes: tonic and bursting. It was originally suggested that bursting occurs only during states such as slow-wave sleep, when little or no information is relayed by the thalamus. However, bursting occurs during wakefulness in the visual and somatosensory thalamus, and could theoretically influence sensory processing. Here we used chronically implanted electrodes to record from the ventroposterior medial thalamic nucleus (VPM) and primary somatosensory cortex (SI) of awake, freely moving rats during different behaviors. These behaviors included quiet immobility, exploratory whisking (large-amplitude whisker movements), and whisker twitching (small-amplitude, 7-to 12-Hz whisker movements). We demonstrated that thalamic bursting appeared during the oscillatory activity occurring before whisker twitching movements, and continued throughout the whisker twitching. Further, thalamic bursting occurred during whisker twitching substantially more often than during the other behaviors, and a neuron was most likely to respond to a stimulus if a burst occurred Ϸ120 ms before the stimulation. In addition, the amount of cortical area activated was similar to that during whisking. However, when SI was inactivated by muscimol infusion, whisker twitching was never observed. Finally, we used a statistical technique called partial directed coherence to identify the direction of influence of neural activity between VPM and SI, and observed that there was more directional coherence from SI to VPM during whisker twitching than during the other behaviors. Based on these findings, we propose that during whisker twitching, a descending signal from SI triggers thalamic bursting that primes the thalamocortical loop for enhanced signal detection during the whisker twitching behavior. I t has been demonstrated that thalamic relay neurons have two distinct modes of firing. These are the tonic firing mode, in which neurons fire single action potentials, and the bursting mode, in which cells fire bursts of two to seven action potentials (1, 2). During the tonic firing mode, cells respond to stimuli with individual spikes that can closely follow incoming activity (3-5). In contrast, during the burst mode, cells respond to incoming stimuli with bursts that do not directly resemble the afferent activity because the bursts are all-or-nothing events, and there is a long refractory period between bursts (4, 5).It was originally thought that the tonic mode was associated with behavioral states, such as wakefulness and sleep, during which afferent stimuli are readily relayed by the thalamus (3, 6-8). In contrast, the bursting mode was thought to occur only during times when no afferent information was, in theory, transmitted by the thalamus (refs. 1, 9, and 10; see ref. 11 for review), such as during slow-wave sleep, barbiturate anesthesia, and pathological conditions such as seizure activity. However, it has recently been demonstrated that thalamic bursting can occur during awake states as well, in multiple species (12-...

show abstract

Section: The Burst Firing Mode Is Not Limited To Sleep and Pathologicsupporting

confidence: 87%

mentioning

confidence: 99%

Thalamic bursting in rats during different awake behavioral states

Fanselow

Sameshima²,

Baccalá³

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

218

174

View full text Add to dashboard Cite

show abstract

“…Any action potential with a preceding interval of Ն100 ms, followed by action potentials within 4 ms of each other, were all counted as burst mode. We had shown earlier that the basic cellular mechanisms that apply to burst firing for thalamic neurons are also present in the monkey (28). All other action potentials that did not fit into this category were counted as tonic mode.…”

Section: Resultsmentioning

confidence: 99%

Higher-order thalamic relays burst more than first-order relays

Ramcharan

Gnadt

Sherman

2005

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

129

116

View full text Add to dashboard Cite

There is a strong correlation between the behavior of an animal and the firing mode (burst or tonic) of thalamic relay neurons. Certain differences between first-and higher-order thalamic relays (which relay peripheral information to the cortex versus information from one cortical area to another, respectively) suggest that more bursting might occur in the higher-order relays. Accordingly, we recorded bursting behavior in single cells from awake, behaving rhesus monkeys in first-order (the lateral geniculate nucleus, the ventral posterior nucleus, and the ventral portion of the medial geniculate nucleus) and higher-order (pulvinar and the medial dorsal nucleus) thalamic relays. We found that the extent of bursting was dramatically greater in the higher-order than in the first-order relays, and this increased bursting correlated with lower spontaneous activity in the higher-order relays. If bursting effectively signals the introduction of new information to a cortical area, as suggested, this increased bursting may be more important in corticocortical transmission than in transmission of primary information to cortex. pulvinar ͉ lateral geniculate nucleus ͉ medial dorsal nucleus ͉ medial geniculate nucleus ͉ ventral posterior nucleus A key feature of the thalamus is the ability of its relay cells to fire in two distinct modes (called tonic and burst), and the firing mode is determined by the inactivation state of voltagegated, T-type Ca 2ϩ channels in the membranes of the soma and dendrites (1-3). This firing mode strongly affects the nature of the signal that is relayed to the cortex (4). For example, compared with tonic mode, burst mode produces much more nonlinear distortion in the relay of information, but the information relayed has greater detectability because of a greater signal-to-noise ratio and stronger activation of postsynaptic cortical targets (4-9). From these properties, the hypothesis has been forwarded that burst firing, with its greater detectability and cortical activation, serves as a ''wake-up call'' to the cortex that there has been a change in the outside world (e.g., a novel stimulus within the receptive field of a relay cell for one of the sensory thalamic nuclei); tonic mode, with its more linear relay of information, is then better suited for a more faithful analysis of the relayed information (4, 7). Thus, burst mode would be more effective for cells dealing with information that is not fully attended to, and the burst would help to redirect attention to the novel stimulus and, ultimately, lead to a shift in firing to tonic mode.Evidence of burst and tonic firing has been reported in various species during waking behavior, including cats (10-12), rats (13-16), guinea pigs (17, 18), rabbits (5, 6), monkeys (19), and humans (20)(21)(22). In general, bursting is relatively rare during full wakefulness and more common during periods of inattention or drowsiness (6). However, nearly all of these data were obtained from cells in first-order thalamic relays, namely, the lateral geniculate nu...

show abstract

“…These authors showed that Ͼ98% of "bursts" identified using these criteria were attributable to LTS activity. Given that LTS activity and burst firing appear rather conserved across different mammalian species (Jahnsen and Llinas, 1984;McCormick and Feeser, 1990;Zhan et al, 1999;Ramcharan et al, 2000), including mice (Kim et al, 2001), the same criteria were used to identify burst firing in the responses of mouse dLGN neurons here. Specifically, the first action potential in a burst had a preceding silent period of Ն100 msec and a following interspike interval (ISI) of Յ4 msec.…”

Section: Methodsmentioning

confidence: 99%

Visual Response Properties in the Dorsal Lateral Geniculate Nucleus of Mice Lacking the β2 Subunit of the Nicotinic Acetylcholine Receptor

Grubb¹,

Thompson²

2004

J. Neurosci.

View full text Add to dashboard Cite

We present a quantitative description of single-cell visual response properties in the dorsal lateral geniculate nucleus (dLGN) of anesthetized adult mice lacking the ␤2 subunit of the nicotinic acetylcholine receptor (␤2Ϫ/Ϫ) and compare these response properties with data from wild-type animals. Some response features, including all spatial receptive field characteristics and bursting behavior, are entirely normal in ␤2Ϫ/Ϫ dLGN cells. In other respects, the responses of ␤2Ϫ/Ϫ dLGN cells are quantitatively abnormal: the mutation is associated with higher spontaneous and visually evoked firing rates, faster visual response latencies, a preference for higher temporal frequencies, and a trend toward greater contrast sensitivity. The normal response properties in the ␤2Ϫ/Ϫ dLGN show that none of the many effects of the mutation, including disrupted geniculate functional organization and abnormal cholinergic transmission, have any effect on spatial response characteristics and bursting behavior in dLGN neurons. The abnormal response characteristics in the ␤2Ϫ/Ϫ dLGN are most interesting in that they are no worse than normal; any visual processing deficits found in studies of the ␤2Ϫ/Ϫ visual cortex must therefore arise solely from abnormalities in cortical processing.

show abstract

Cellular Mechanisms Underlying Activity Patterns in the Monkey Thalamus During Visual Behavior

Cited by 43 publications

References 24 publications

Thalamic bursting in rats during different awake behavioral states

Thalamic bursting in rats during different awake behavioral states

Higher-order thalamic relays burst more than first-order relays

Visual Response Properties in the Dorsal Lateral Geniculate Nucleus of Mice Lacking the β2 Subunit of the Nicotinic Acetylcholine Receptor

Contact Info

Product

Resources

About